Micro RNA-137/181c regulates serine palmitoyltransferase and in turn amyloid β novel targets in sporadic Alzheimer's disease

Journal of Neuroscience

Volumn 31, Issue 41, 2011, Pages 14820-14830

  Geekiyanage, Hirosha ^a   Chan, Christina ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; MICRORNA; MIR 137; MIR 181C; MIR 29A; MIR 29B 1; MIR 9; SERINE PALMITOYLTRANSFERASE; UNCLASSIFIED DRUG; AMYLOID PRECURSOR PROTEIN; CERAMIDE; MIRN137 MICRORNA, HUMAN; MIRN181 MICRORNA, HUMAN; SPHINGOMYELIN; SPTLC1 PROTEIN, HUMAN; SPTLC2 PROTEIN, HUMAN;

AGE DISTRIBUTION; AGED; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENE FUNCTION; GENE LOSS; GENETIC REGULATION; HUMAN; HUMAN TISSUE; LIPID DIET; MALE; MOUSE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; RISK FACTOR; SEX DIFFERENCE; UPREGULATION; AGE; ANIMAL; ASTROCYTE; BRAIN; C57BL MOUSE; CADAVER; CELL CULTURE; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; MUTATION; NEWBORN; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; STATISTICS; TRANSGENIC MOUSE;

AGE FACTORS; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BRAIN; CELLS, CULTURED; CERAMIDES; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; MUTATION; POSTMORTEM CHANGES; RATS; RATS, SPRAGUE-DAWLEY; SERINE C-PALMITOYLTRANSFERASE; SEX FACTORS; SPHINGOMYELINS; STATISTICS AS TOPIC; TRANSFECTION;

EID: 80054025163     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3883-11.2011     Document Type: Article

References (61)

1. An JH, Lee SY, Jeon JY, Cho KG, Kim SU, Lee MA (2009) Identification of gliotropic factors that induce human stem cell migration to malignant tumor. J Proteome Res 8:2873-2881.
2. Androulidaki A, Iliopoulos D, Arranz A, Doxaki C, Schworer S, Zacharioudaki V, Margioris AN, Tsichlis PN, Tsatsanis C (2009) The kinase Akt1 controls macrophage response to lipopolysaccharide by regulating microRNAs. Immunity 31:220-231.
3. Bachman DL, Wolf PA, Linn R, Knoefel JE, Cobb J, Belanger A, D'Agostino RB, White LR (1992) Prevalence of dementia and probable senile dementia of the Alzheimer type in the Framingham Study. Neurology 42:115-119.
4. Bandaru VV, Troncoso J, Wheeler D, Pletnikova O, Wang J, Conant K, Haughey NJ (2009) ApoE4 disrupts sterol and sphingolipid metabolism in Alzheimer's but not normal brain. Neurobiol Aging 30:591-599.
5. Betel D, Wilson M, Gabow A, Marks DS, Sander C (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res 36:D149-153.
6. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911-917.
7. Butler AW, Ng MY, Hamshere ML, Forabosco P, Wroe R, Al-Chalabi A, Lewis CM, Powell JF (2009) Meta-analysis of linkage studies for Alzheimer's disease-a web resource. Neurobiol Aging 30:1037-1047.
8. Chang ZQ, Lee SY, Kim HJ, Kim JR, Kim SJ, Hong IK, Oh BC, Choi CS, Goldberg IJ, Park TS (2011) Endotoxin activates de novo sphingolipid biosynthesis via nuclear factor kappa B-mediated upregulation of Sptlc2. Prostaglandins Other Lipid Mediat 94:44-52.
9. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, Strome R, Zuker N, Loukides J, French J, Turner S, Lozza G, Grilli M, Kunicki S, Morissette C, Paquette J, Gervais F, Bergeron C, Fraser PE, Carlson GA, et al. (2001) Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 276:21562-21570.
10. Cogswell JP, Ward J, Taylor IA, Waters M, Shi Y, Cannon B, Kelnar K, Kemppainen J, Brown D, Chen C, Prinjha RK, Richardson JC, Saunders AM, Roses AD, Richards CA (2008) Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J Alzheimers Dis 14:27-41.
11. Coolen M, Bally-Cuif L (2009) MicroRNAs in brain development and physiology. Curr Opin Neurobiol 19:461-470.
12. Cordy JM, Hussain I, Dingwall C, Hooper NM, Turner AJ (2003) Exclusively targeting beta-secretase to lipid rafts by GPI-anchor addition upregulates beta-site processing of the amyloid precursor protein. Proc Natl Acad Sci U S A 100:11735-11740.
13. Cortez MA, Nicoloso MS, Shimizu M, Rossi S, Gopisetty G, Molina JR, Carlotti C Jr, Tirapelli D, Neder L, Brassesco MS, Scrideli CA, Tone LG, Georgescu MM, Zhang W, Puduvalli V, Calin GA (2010) miR-29b and miR-125a regulate podoplanin and suppress invasion in glioblastoma. Genes Chromosomes Cancer 49:981-990.
14. Costantini C, Ko MH, Jonas MC, Puglielli L (2007) A reversible form of lysine acetylation in the ER and Golgi lumen controls the molecular stabilization of BACE1. The Biochemical journal 407:383-395.
15. Cruts M, Van Broeckhoven C (1998) Molecular genetics of Alzheimer's disease. Ann Med 30:560-565.
16. Cutler RG, Kelly J, Storie K, Pedersen WA, Tammara A, Hatanpaa K, Troncoso JC, Mattson MP (2004) Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc Natl Acad Sci U S A 101:2070-2075.
17. Ebina M, Futai E, Tanabe C, Sasagawa N, Kiso Y, Ishiura S (2009) Inhibition by KMI-574 leads to dislocalization of BACE1 from lipid rafts. J Neurosci Res 87:360-368.
18. Gao FB (2010) Context-dependent functions of specific microRNAs in neuronal development. Neural Dev 5:25
19. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36:D154-158.
20. Haas RH, Rice MA, Trauner DA, Merritt TA (1986) Therapeutic effects of a ketogenic diet in Rett syndrome. Am J Med Genet Suppl 1:225-246.
21. Han X, Holtzman DM, McKeel DW Jr, Kelley J, Morris JC (2002) Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer's disease: potential role in disease pathogenesis. J Neurochem 82:809-818.
22. Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9:139-150.
23. He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522-531.
24. He X, Huang Y, Li B, Gong CX, Schuchman EH (2010) Deregulation of sphingolipid metabolism in Alzheimer's disease. Neurobiol Aging 31:398-408.
25. Hébert SS, Horré K, Nicolaï L, Papadopoulou AS, Mandemakers W, Silahtaroglu AN, Kauppinen S, Delacourte A, De Strooper B (2008) Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc Natl Acad Sci U S A 105:6415-6420.
26. Hojjati MR, Li Z, Zhou H, Tang S, Huan C, Ooi E, Lu S, Jiang XC (2005) Effect of myriocin on plasma sphingolipid metabolism and atherosclerosis in apoE-deficient mice. J Biol Chem 280:10284-10289.
27. Hornemann T, Richard S, Rütti MF, Wei Y, von Eckardstein A (2006) Cloning and initial characterization of a new subunit for mammalian serinepalmitoyltransferase. J Biol Chem 281:37275-37281.
28. Inoue M, Ohtake T, Motomura W, Takahashi N, Hosoki Y, Miyoshi S, Suzuki Y, Saito H, Kohgo Y, Okumura T (2005) Increased expression of PPARgamma in high fat diet-induced liver steatosis in mice. Biochem Biophys Res Commun 336:215-222.
29. Jana A, Pahan K (2010) Fibrillar amyloid-beta-activated human astroglia kill primary human neurons via neutral sphingomyelinase: implications for Alzheimer's disease. J Neurosci 30:12676-12689.
30. Julien C, Tremblay C, Phivilay A, Berthiaume L, Emond V, Julien P, Calon F (2010) High-fat diet aggravates amyloid-beta and tau pathologies in the 3xTg-AD mouse model. Neurobiol Aging 31:1516-1531.
31. Ko MH, Puglielli L (2009) Two endoplasmic reticulum (ER)/ER Golgi intermediate compartment-based lysine acetyltransferases post-translationally regulate BACE1 levels. J Biol Chem 284:2482-2492.
32. Koturbash I, Zemp F, Kolb B, Kovalchuk O (2011) Sex-specific radiationinduced microRNAome responses in the hippocampus, cerebellum and frontal cortex in a mouse model. Mutat Res 722:114-118.
33. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N (2005) Combinatorial microRNA target predictions. Nat Genet 37:495-500.
34. Ladisch S, Li R, Olson E (1994) Ceramide structure predicts tumor ganglioside immunosuppressive activity. Proc Natl Acad Sci U S A 91: 1974-1978.
35. Laneve P, Gioia U, Andriotto A, Moretti F, Bozzoni I, Caffarelli E (2010) A minicircuitry involving REST and CREB controls miR-9-2 expression during human neuronal differentiation. Nucleic Acids Res 38:6895-6905.
36. Langevin SM, Stone RA, Bunker CH, Grandis JR, Sobol RW, Taioli E (2010) MicroRNA-137 promoter methylation in oral rinses from patients with squamous cell carcinoma of the head and neck is associated with gender and body mass index. Carcinogenesis 31:864-870.
37. Lee SJ, Liyanage U, Bickel PE, Xia W, Lansbury PT Jr, Kosik KS (1998) A detergent-insoluble membrane compartment containsAbeta in vivo. Nat Med 4:730-734.
38. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20.
39. Liebhaber GM, Riemann E, Baumeister FA (2003) Ketogenic diet in Rett syndrome. J Child Neurol 18:74-75.
40. Lukiw WJ (2007) Micro-RNA speciation in fetal, adult and Alzheimer's disease hippocampus. Neuroreport 18:297-300.
41. Mattson MP, Cutler RG, Jo DG (2005) Alzheimer peptides perturb lipidregulating enzymes. Nat Cell Biol 7:1045-1047.
42. Mehler MF, Mattick JS (2006) Non-coding RNAs in the nervous system. J Physiol 575:333-341.
43. Memon RA, Holleran WM, Uchida Y, Moser AH, Grunfeld C, Feingold KR (2001) Regulation of sphingolipid and glycosphingolipid metabolism in extrahepatic tissues by endotoxin. J Lipid Res 42:452-459.
44. Niwa R, Zhou F, Li C, Slack FJ (2008) The expression of the Alzheimer's amyloid precursor protein-like gene is regulated by developmental timing microRNAs and their targets in Caenorhabditis elegans. Dev Biol 315:418-425.
45. Patil S, Melrose J, Chan C (2007) Involvement of astroglial ceramide in palmitic acid-induced Alzheimer-like changes in primary neurons. Eur J Neurosci 26:2131-2141.
46. Perry DK, Carton J, Shah AK, Meredith F, Uhlinger DJ, Hannun YA (2000) Serine palmitoyltransferase regulates de novo ceramide generation during etoposide-induced apoptosis. J Biol Chem 275:9078-9084.
47. Pettegrew JW, Panchalingam K, Hamilton RL, McClure RJ (2001) Brain membrane phospholipid alterations in Alzheimer's disease. Neurochem Res 26:771-782.
48. Puglielli L, Ellis BC, Saunders AJ, Kovacs DM (2003) Ceramide stabilizes beta-site amyloid precursor protein-cleaving enzyme 1 and promotes amyloid beta-peptide biogenesis. J Biol Chem 278:19777-19783.
49. Rotthier A, Auer-Grumbach M, Janssens K, Baets J, Penno A, Almeida-Souza L, Van Hoof K, Jacobs A, De Vriendt E, Schlotter-Weigel B, Löscher W, Vondráček P, Seeman P, De Jonghe P, Van Dijck P, Jordanova A, Hornemann T, Timmerman V (2010) Mutations in the SPTLC2 subunit of serine palmitoyltransferase cause hereditary sensory and autonomic neuropathy type I. Am J Hum Genet 87:513-522.
50. Scarlatti F, Sala G, Somenzi G, Signorelli P, Sacchi N, Ghidoni R (2003) Resveratrol induces growth inhibition and apoptosis in metastatic breast cancer cells via de novo ceramide signaling. FASEB J 17:2339-2341.
51. Schonrock N, Ke YD, Humphreys D, Staufenbiel M, Ittner LM, Preiss T, Götz J (2010) Neuronal microRNA deregulation in response to Alzheimer's disease amyloid-beta. PloS one 5:e11070.
52. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439:283-289.
53. Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V (2004) Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome biology 5:R13.
54. Shah C, Yang G, Lee I, Bielawski J, Hannun YA, Samad F (2008) Protection from high fat diet-induced increase in ceramide in mice lacking plasminogen activator inhibitor 1. J Biol Chem 283:13538-13548.
55. Shioya M, Obayashi S, Tabunoki H, Arima K, Saito Y, Ishida T, Satoh J (2010) Aberrant microRNA expression in the brains of neurodegenerative diseases: miR-29a decreased in Alzheimer disease brains targets neurone navigator 3. Neuropathol Appl Neurobiol 36:320-330.
56. Szulwach KE, Li X, Smrt RD, Li Y, Luo Y, Lin L, Santistevan NJ, Li W, Zhao X, Jin P (2010) Cross talk between microRNA and epigenetic regulation in adult neurogenesis. J Cell Biol 189:127-141.
57. Tremblay F, Lavigne C, Jacques H, Marette A (2001) Defective insulininduced GLUT4 translocation in skeletal muscle of high fat-fed rats is associated with alterations in both Akt/protein kinase B and atypical protein kinase C (zeta/lambda) activities. Diabetes 50:1901-1910.
58. Valsecchi M, Mauri L, Casellato R, Prioni S, Loberto N, Prinetti A, Chigorno V, Sonnino S (2007) Ceramide and sphingomyelin species of fibroblasts and neurons in culture. J Lipid Res 48:417-424.
59. Vetrivel KS, Cheng H, Kim SH, Chen Y, Barnes NY, Parent AT, Sisodia SS, Thinakaran G (2005) Spatial segregation of gamma-secretase and substrates in distinct membrane domains. J Biol Chem 280:25892-25900.
60. Wang WX, Rajeev BW, Stromberg AJ, Ren N, Tang G, Huang Q, Rigoutsos I, Nelson PT (2008) The expression of microRNA miR-107 decreases early in Alzheimer's disease and may accelerate disease progression through regulation of β-site amyloid precursor protein-cleaving enzyme 1. J Neurosci 28:1213-1223.
61. Zhang J, Zhang F, Didelot X, Bruce KD, Cagampang FR, Vatish M, Hanson M, Lehnert H, Ceriello A, Byrne CD (2009) Maternal high fat diet during pregnancy and lactation alters hepatic expression of insulin like growth factor-2 and key microRNAs in the adult offspring. BMC Genomics 10:478.